Abstract

There have been intense debates over the geographic origin of African crops and agriculture. Here, we used whole-genome sequencing data to infer the domestication origin of pearl millet (Cenchrus americanus). Our results supported an origin in western Sahara, and we dated the onset of cultivated pearl millet expansion in Africa to 4,900 years ago. We provided evidence that wild-to-crop gene flow increased cultivated genetic diversity leading to diversity hotspots in western and eastern Sahel and adaptive introgression of 15 genomic regions. Our study reconciled genetic and archaeological data for one of the oldest African crops.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Vavilov, N. I. & Dorofeev, V. F. Origin and Geography of Cultivated Plants (Cambridge Univ. Press, Cambridge, 1992).

  2. 2.

    Harlan, J. R., De Wet, J. M. J. & Stemler, A. B. L. Origins of African Plant Domestication (De Gruyter, Berlin, 1976).

  3. 3.

    Harlan, J. R. Science 174, 468–474 (1971).

  4. 4.

    Varshney, R. K. et al. Nat. Biotechnol. 35, 969–976 (2017).

  5. 5.

    Hu, Z. et al. BMC Genom. 16, 1048 (2015).

  6. 6.

    Dussert, Y., Snirc, A. & Robert, T. Mol. Ecol. 24, 1387–1402 (2015).

  7. 7.

    Manning, K. in West African Archaeology: New Developments, New Perspectives (ed. Allsworth-Jones, P.) 43–52 (Archaeopress, Oxford, 2010).

  8. 8.

    Manning, K., Pelling, R., Higham, T., Schwenniger, J.-L. & Fuller, D. Q. J. Archaeol. Sci. 38, 312–322 (2011).

  9. 9.

    Ozainne, S. et al. J. Archaeol. Sci. 50, 359–368 (2014).

  10. 10.

    Oumar, I., Mariac, C., Pham, J.-L. & Vigouroux, Y. Theor. Appl. Genet. 117, 489–497 (2008).

  11. 11.

    Berthouly-Salazar, C. et al. Front. Plant Sci. 7, 777 (2016).

  12. 12.

    Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C. & Foll, M. PLoS Genet. 9, e1003905 (2013).

  13. 13.

    Cubry, P., Vigouroux, Y. & François, O. Front. Genet. 8, 139 (2017).

  14. 14.

    Reich, D., Thangaraj, K., Patterson, N., Price, A. L. & Singh, L. Nature 461, 489–494 (2009).

  15. 15.

    Pickrell, J. K. & Pritchard, J. K. PLOS Genet. 8, e1002967 (2012).

  16. 16.

    Kröpelin, S. et al. Science 320, 765–768 (2008).

  17. 17.

    Huerta-Sánchez, E. et al. Nature 512, 194–197 (2014).

  18. 18.

    Ai, H. et al. Nat. Genet. 47, 217–225 (2015).

  19. 19.

    Arnold, B. J. et al. Proc. Natl Acad. Sci. USA 113, 8320–8325 (2016).

  20. 20.

    Hufford, M. B. et al. PLoS Genet. 9, e1003477 (2013).

  21. 21.

    Nielsen, R. et al. Genome Res. 15, 1566–1575 (2005).

  22. 22.

    Dupuy, C. Encycl. Berbère XXXIX, 6529–6544 (2015).

  23. 23.

    Frichot, E., Mathieu, F., Trouillon, T., Bouchard, G. & François, O. Genetics 196, 973–983 (2014).

  24. 24.

    Frichot, E. & François, O. Methods Ecol. Evol. 6, 925–929 (2015).

  25. 25.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2016).

  26. 26.

    Caye, K., Deist, T. M., Martins, H., Michel, O. & François, O. Mol. Ecol. Resour. 16, 540–548 (2016).

  27. 27.

    Excoffier, L. & Foll, M. Bioinformatics 27, 1332–1334 (2011).

  28. 28.

    Ray, N., Currat, M., Foll, M. & Excoffier, L. Bioinformatics 26, 2993–2994 (2010).

  29. 29.

    Csilléry, K., Blum, M. G. B., Gaggiotti, O. E. & François, O. Trends Ecol. Evol. 25, 410–418 (2010).

  30. 30.

    Csilléry, K., François, O. & Blum, M. G. B. Methods Ecol. Evol. 3, 475–479 (2012).

  31. 31.

    Nielsen, R. et al. PLoS Biol. 3, e170 (2005).

  32. 32.

    Pavlidis, P., Živković, D., Stamatakis, A. & Alachiotis, N. Mol. Biol. Evol. 30, 2224–2234 (2013).

  33. 33.

    Weir, B. S. Genetic Data Analysis II: Methods for Discrete Population Genetic Data (Oxford Univ. Press, Oxford, 1996).

  34. 34.

    Weir, B. S. & Cockerham, C. C. Evolution 38, 1358–1370 (1984).

  35. 35.

    Nei, M. & Li, W. H. Proc. Natl Acad. Sci. USA 76, 5269–5273 (1979).

  36. 36.

    Cruickshank, T. E. & Hahn, M. W. Mol. Ecol. 23, 3133–3157 (2014).

  37. 37.

    Bass, J. D., Dabney, A. & Robinson, D. qvalue: Q-value Estimation for False Discovery Rate Control R package version 2.12.0 (2015).

Download references

Acknowledgements

We are grateful to the Genotoul sequencing platform Toulouse Midi-Pyrenees for help during sequencing. We also want to thank N. Tando and the IRD itrop Plantes Santé bioinformatic platform for providing HPC resources and support for our research project. Y.V. acknowledges support from the Agence Nationale de la Recherche (ANR-13-BSV7-0017). C.B.-S. acknowledges support from Agropolis Fondation under the reference ID 1403-057 through the Investissements d’avenir programme (Labex Agro: ANR-10-LABX-0001-01).

Author information

Author notes

  1. These authors contributed equally to this work: Concetta Burgarella, Philippe Cubry.

Affiliations

  1. IRD, Université Montpellier, DIADE, Montpellier, France

    • Concetta Burgarella
    • , Philippe Cubry
    • , Cedric Mariac
    • , Marie Couderc
    • , Nora Scarcelli
    • , Adeline Barnaud
    • , Bénédicte Rhoné
    • , Cécile Berthouly-Salazar
    •  & Yves Vigouroux
  2. AGAP, Université Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France

    • Concetta Burgarella
  3. Senegalese Agricultural Research Institute, Dakar, Senegal

    • Ndjido A. Kane
    •  & Cécile Berthouly-Salazar
  4. Laboratoire Mixte International LAPSE, Dakar, Senegal

    • Ndjido A. Kane
    •  & Adeline Barnaud
  5. Center of Excellence in Genomics and Systems Biology, International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, Telangana, India

    • Rajeev K. Varshney
    • , Mahendar Thudi
    •  & Annapurna Chitikineni
  6. BGI-Shenzhen, Shenzhen, China

    • Xin Liu
    • , Chengcheng Shi
    •  & Xun Xu
  7. Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive, Lyon, France

    • Bénédicte Rhoné
  8. Institut des Mondes Africains, Paris, France

    • Christian Dupuy
  9. Université Grenoble-Alpes, Centre National de la Recherche Scientifique, Grenoble, France

    • Olivier François

Authors

  1. Search for Concetta Burgarella in:

  2. Search for Philippe Cubry in:

  3. Search for Ndjido A. Kane in:

  4. Search for Rajeev K. Varshney in:

  5. Search for Cedric Mariac in:

  6. Search for Xin Liu in:

  7. Search for Chengcheng Shi in:

  8. Search for Mahendar Thudi in:

  9. Search for Marie Couderc in:

  10. Search for Xun Xu in:

  11. Search for Annapurna Chitikineni in:

  12. Search for Nora Scarcelli in:

  13. Search for Adeline Barnaud in:

  14. Search for Bénédicte Rhoné in:

  15. Search for Christian Dupuy in:

  16. Search for Olivier François in:

  17. Search for Cécile Berthouly-Salazar in:

  18. Search for Yves Vigouroux in:

Contributions

C.B., P.C., N.A.K., A.B., O.F., C.B.-S. and Y.V. designed the analysis. C.B. and P.C. performed statistical analyses. C.M. and M.C. performed additional experimental work. B.R., N.S., C.D., M.T., C.S. and O.F. contributed to analytic tools, data, methods and participated in data analysis; X.L., X.X., R.K.V. and Y.V. managed and designed the pearl millet genome project. O.F., C.B.-S. and Y.V. managed this genomic diversity study. C.B., P.C., C.B.-S. and Y.V. wrote the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Concetta Burgarella or Philippe Cubry or Olivier François or Cécile Berthouly-Salazar or Yves Vigouroux.

Supplementary information

  1. Supplementary Information

    Supplementary data, models, references, tables and figures

  2. Reporting Summary

  3. Supplementary Table 1

    Passport data

  4. Supplementary Table 7

    Gene models and annotation for genomic regions under selection

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41559-018-0643-y